The central focus of my research is to understand the pattern and processes of trait evolution through long time scales using phylogenetic trees. My research is divided into development of new phylogenetic comparative models of trait evolution and empirical studies of macroevolution with multiple study systems.One of the big questions in macroevolution is what drives and maintains biodiversity among clades and through time. This question is frequently addressed by studying the dynamics of diversification; how fast species accumulate and how frequently they go extinct. However, the phenotype diversity of lineages is a fundamental component of biodiversity and cannot be predicted by species dynamics alone. For example, some clades are speciose but lack morphological diversity (e.g., cryptic species) while others show great morphological disparity. Thus, in order to understand macroevolutionary patterns and processes across the tree of life, we need to study the dynamics of trait evolution.

Phylogenies and evolutionary integration among traits

Correlated evolution among traits (known as evolutionary integration) has an important impact on the trajectory of phenotypic evolution. Genetic constraints, ontogeny, and selection have pivotal roles in the development and maintenance of morphological integration over time. Furthermore, shifts in the pattern of evolutionary integration among traits over macroevolutionary scales may play a fundamental role in the evolution of novel phenotypes through exploration of unoccupied regions of morphospace. However, most of what we know about the tempo and mode of trait evolution come from studies that consider only single traits or that use principal component analysis (PCA) to reduce the dimensionality of the data. Studying traits individually excludes the possibility of identifying patterns of evolutionary correlation and the use of PCA does not allow testing for evolutionary shifts in integration. More specifically, we have shown that PCA and phylogenetic PCA (pPCA) can bias the biological interpretation of the mode of evolution underlying the data (Uyeda, Caetano and Pennell, 2015; Systematic Biology) because statistical properties of these methods lead to the first PC axes consistently being estimated as early bursts of differentiation whereas the last axes store a strong signal of stabilizing selection, regardless of the true model.

Therefore, we need models that apply to multivariate data as such in order to better understand macroevolutionary patterns of evolutionary integration. To accomplish that, I have developed a novel framework to facilitate the study of evolutionary integration among traits using phylogenetic trees. The central idea is to estimate rates of evolution for each individual trait in a dataset while also evaluating the structure of evolutionary correlation among them. With this model one can also fit different rate regimes to the phylogenetic tree and detect shifts between regimes due to distinct patterns of evolutionary rates and/or correlations among traits (Caetano and Harmon, under review in Systematic Biology). I implemented this approach in the R package 'ratematrix', that is already available for use (Caetano and Harmon, under review in Methods in Ecology and Evolution – and available at github ).

Long standing questions under new perspectives

Some big questions in macroevolution have been asked for a many years using different approaches, but modern comparative methods often provide the ideal framework. Phylogenetic comparative methods allow us to test hypotheses based on the pattern of evolution of traits and lineages. I use this approach to address a series of questions in evolutionary biology with a rigorous phylogenetic component.

Do male genitalia evolve faster than female genitalia? The striking diversity of genitalia shape and size observed in most animal groups has often been associated with sexual selection or species reinforcement. However, female genitalia is often ignored and its evolutionary dynamics are poorly understood, most likely because male genitalia are easier to observe and therefore used as species-level taxonomic characters for many groups. This bias has produced a generalized but largely untested notion that male genitalia evolves faster than female genitalia, usually relying solely on taxonomic information and without formally considering phylogenetic relationships. We tested this hypothesis using novel and explicit macroevolutionary models in a clade of stink bugs (Genevcius, Caetano and Schwertner, 2017; Journal of Evolutionary Biology). In this paper we show that male and female genitalia co-evolve, that both evolve much faster than somatic traits and that male genitalia do evolve faster than female genitalia.

Does aposematic mimicry influence diversification? Mimics of aposematic species are thought to avoid predation by deceiving predators. In snakes, for example, experiments in the field have shown that bird predators avoid snake-form models with aposematic coloration. Such decrease in predation pressure, compared to non-mimic populations could lead to faster accumulation of new species over time. In order to test this hypothesis, I teamed up with herpetologists to investigate whether false-coral snakes of the Neotropical family Dipsadidae show higher diversification rates than non-mimic lineages within the same group (Caetano et al., 2016; BioRxiv preprint). We showed that there is no difference between the net diversification rates of mimic and non-mimic lineages. Surprisingly, the once thought clear advantage of mimic species has no consistent effect on lineage diversification in the group.